Screening of broad spectrum natural pesticides against conserved target arginine kinase in cotton pests by molecular modeling

Journal of Biomolecular Structure and Dynamics

Volumn 37, Issue 4, 2019, Pages 1022-1042

  Sakthivel, Seethalakshmi ^a   Habeeb, S K M ^a   Raman, Chandrasekar ^b  

^a SRM INSTITUTE OF SCIENCE AND TECHNOLOGY   (India)

^b KANSAS STATE UNIVERSITY   (United States)

Author keywords

Aphis gossypii; arginine kinase; cotton; expressed sequence tags; Helicoverpa armigera; HTVS; insecticide resistance; molecular dynamics; orthologous target; Spodoptera exigua

Indexed keywords

ARGININE KINASE; PESTICIDE; INSECT PROTEIN;

ARTICLE; COTTON APHID; CROP PEST; ENERGY METABOLISM; HELICOVERPA ARMIGERA; HYDROGEN BOND; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN TARGETING; SEQUENCE ANALYSIS; SPODOPTERA EXIGUA; SURFACE AREA; ANIMAL; CHEMISTRY; DRUG DATABASE; DRUG EFFECT; ENZYMOLOGY; GENETICS; GOSSYPIUM; HIGH THROUGHPUT SCREENING; PARASITOLOGY; PROCEDURES; PROTEIN CONFORMATION; SPODOPTERA;

ANIMALS; ARGININE KINASE; DATABASES, PHARMACEUTICAL; GOSSYPIUM; HIGH-THROUGHPUT SCREENING ASSAYS; INSECT PROTEINS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; PESTICIDES; PROTEIN CONFORMATION; SPODOPTERA;

EID: 85043470002     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2018.1447514     Document Type: Article

References (65)

1. Adams, M. D., Kelley, J. M., Gocayne, J. D., Dubnick, M., Polymeropoulos, M. H., Xiao, H., … Moreno, R. F., (1991). Complementary DNA sequencing: Expressed sequence tags and human genome project. Science, 252(5013), 1651–1656. doi:10.1126/science.2047873
2. Ahmad, S., Gromiha, M. M., & Sarai, A., (2004). Analysis and prediction of DNA-binding proteins and their binding residues based on composition, sequence and structural information. Bioinformatics, 20(4), 477–486. doi:10.1093/bioinformatics/btg432
3. Aslam, M., Razaq, M., Shah, S. A., & Ahmad, F., (2004). Comparative efficacy of different insecticides against sucking pests of cotton. Journal of Research (Science), 15(1), 53–58. doi:10.1007/s13398-014-0173-7.2
4. Audsley, N., & Down, R. E., (2015). G protein coupled receptors as targets for next generation pesticides. Insect Biochemistry and Molecular Biology, 67, 27–37. doi:10.1016/j.ibmb.2015.07.014
5. Banavath, H. N., Sharma, O. P., Kumar, M. S., & Baskaran, R., (2014). Identification of novel tyrosine kinase inhibitors for drug resistant T315I mutant BCR-ABL: A virtual screening and molecular dynamics simulations study. Scientific Reports, 4, 6498. doi:10.1038/srep06948
6. Barrett, M. P., Mottram, J. C., & Coombs, G. H., (1999). Recent advances in identifying and validating drug targets in trypanosomes and leishmanias. Trends in Microbiology, 7(2), 82–88. doi:10.1016/S0966-842X(98)01433-4
7. Bera, K., Rani, P., Kishor, G., Agarwal, S., & Singh, D. V., (2017, September). Structural elucidation of transmembrane domain zero (TMD0) of EcdL: A multidrug resistance- associated protein (MRP) family of ATP-binding cassette transporter protein revealed by atomistic simulation. Journal of Biomolecular Structure and Dynamics, 1102, 1–13. doi:10.1080/07391102.2017.1372311
8. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R., (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. doi:10.1063/1.448118
9. Blethen, S. L., (1972). Kinetic properties of the arginine kinase isoenzymes of Limulus polyphemus. Archives of Biochemistry and Biophysics, 149(1), 244–251. doi:10.1016/0003-9861(72)90319-0
10. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L., (2009). BLAST plus: Architecture and applications. BMC Bioinformatics, 10(421), 1. http://doi.org/Artn421\n. Doi 10.1186/1471-2105-10-421
11. Catarino, R., Ceddia, G., Areal, F. J., & Park, J., (2015). The impact of secondary pests on Bacillus thuringiensis (Bt) crops. Plant Biotechnology Journal, 13(5), 601–612. doi:10.1111/pbi.12363
12. Colovos, C., Yeates, T. O., (1993). Verification of protein structure: Patterns of nonbonded atomic interactions. Protein Science, 2, 1511–1519.10.1002/pro.v2:9
13. Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J., Talon, M., & Robles, M., (2005). Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18), 3674–3676. doi:10.1093/bioinformatics/bti610
14. David, J., Ismail, H. M., Chandor-proust, A., John, M., Paine, I., John, M., & Paine, I., (2013). Role of cytochrome P450s in insecticide resistance : Impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philosophical Transactions of the Royal Society of London, 368, 20120429.
15. Deng, F., Xie, M., Zhang, X., Li, P., Tian, Y., Zhai, H., & Li, Y., (2014). Combined molecular docking, molecular dynamics simulation and quantitative structure–Activity relationship study of pyrimido[1,2-c][1,3]benzothiazin-6-imine derivatives as potent anti-HIV drugs. Journal of Molecular Structure, 1067, 1–13. doi:10.1016/j.molstruc.2014.03.008
16. Dhillon, M. K., & Sharma, H. C., (2013). Comparative studies on the effects of Bt-transgenic and non-transgenic cotton on arthropod diversity, seedcotton yield and bollworms control. Journal of Environmental Biology, 34(1), 67–73.
17. Doz, P., Selzer, P. M., Marhöfer, R. J., & Rohwer, A., (2004). Angewandte bioinformatik. Berlin: Springer-Lehrbuch.
18. Ellington, W. R., (2001). Evolution and physiological roles of phosphagen systems. Annual Review of Physiology, 63(1), 289–325. doi:10.1146/annurev.physiol.63.1.289
19. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G., (1995). A smooth particle mesh Ewald method. The Journal of Chemical Physics, 103(19), 8577–8593. doi:10.1063/1.470117
20. Gasteiger, J., (2006). Chemoinformatics: A new field with a long tradition. Analytical and Bioanalytical Chemistry, 384, 57–64. doi:10.1007/s00216-005-0065-y
21. George, D. C. P., Chakraborty, C., Haneef, S. A. S., & Nagasundaram, N., (2014). Evolution- and structure-based computational strategy reveals the impact of deleterious missense mutations on MODY 2 (Maturity-onset diabetes of the young, Type 2). Theranostics, 4(4), 366–383. doi:10.7150/thno.7473
22. Gerlt, J. A., Kreevoy, M. M., Cleland, W. W., & Frey, P. A., (1997). Understanding enzymic catalysis: The importance of short, strong hydrogen bonds. Chemistry & Biology, 4(4), 259–267. doi:10.1016/S1074-5521(97)90069-7
23. Hemingway, J., Hawkes, N. J., McCarroll, L., & Ranson, H., (2004). The molecular basis of insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology, 34(7), 653–665. doi:10.1016/j.ibmb.2004.03.018
24. Hirose, T., Sunazuka, T., & Ōmura, S., (2010). Recent development of two chitinase inhibitors, Argifin and Argadin, produced by soil microorganisms. Proceedings of the Japan Academy, Series B, 86(2), 85–102. doi:10.2183/pjab.86.85
25. Huang, X., & Madan, A., (1999). CAP 3: A DNA sequence assembly program. Genome Research, 9(9), 868–877. doi:10.1101/gr.9.9.868
26. Insecticide Resistance Action Committee. (2015). IRAC MoA Classification Scheme. MoA Classification V7.4, May ‘15. www.irac-online.org.
27. Irwin, J. J., & Shoichet, B. K., (2005). ZINC − A free database of commercially available compounds for virtual screening. Journal of Chemical Information and Modeling, 45(1), 177–182. doi:10.1021/ci049714+
28. Jeong, K., Lee, J., & Kim, Y., (2007). Homology modeling and docking study of β -ketoacyl acyl carrier protein synthase III from enterococcus faecalis. Bulletin of the Korean Chemical Society, 28(8), 1335–1340.
29. Jiang, J., Zhou, K., Liang, G., Zeng, L., & Wen, S., (2014). A novel point mutation of acetylcholinesterase in a trichlorfon-resistant strain of the oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae). Applied Entomology and Zoology, 49(1), 129–137. doi:10.1007/s13355-013-0232-0
30. Karthick, V., & Ramanathan, K., (2013). Virtual screening for oseltamivir-resistant a (H5N1) influenza neuraminidase from traditional Chinese medicine database: A combined molecular docking with molecular dynamics approach. SpingerPlus, 2(115), 1–10.
31. Kazem, M. G. T., & El-Shereif, S. A. E. H. N., (2010). Toxic effect of capsicum and garlic xylene extracts in toxicity of boiled linseed oil formulations against some piercing sucking cotton pests. American-Eurasian Journal of Agricultural & Environmental Sciences, 8(4), 390–396.
32. Kenyon, G. L., & Reed, G. H., (1983). Creatine kinase: Structure-activity relationships. Advances in Enzymology and Related Areas of Molecular Biology, 54, 367–426.
33. Kesherwani, M., Michael Gromiha, M., Fukui, K., & Velmurugan, D., (2017). Identification of novel natural inhibitor for NorM–A multidrug and toxic compound extrusion transporter–an insilico molecular modeling and simulation studies. Journal of Biomolecular Structure and Dynamics, 35(1), 58–77. doi:10.1080/07391102.2015.1132391
34. Krasky, A., Rohwer, A., Schroeder, J., & Selzer, P. M., (2007). A combined bioinformatics and chemoinformatics approach for the development of new antiparasitic drugs. Genomics, 89(1), 36–43. doi:10.1016/j.ygeno.2006.09.008
35. López-Zavala, A. A., García-Orozco, K. D., Carrasco-Miranda, J. S., Sugich-Miranda, R., Velázquez-Contreras, E. F., Criscitiello, M. F., … Sotelo-Mundo, R. R., (2013). Crystal structure of shrimp arginine kinase in binary complex with arginine–A molecular view of the phosphagen precursor binding to the enzyme. Journal of Bioenergetics and Biomembranes, 45, 511–518. doi:10.1007/s10863-013-9521-0
36. Lu, B., Downes, S., Wilson, L., Gregg, P., Knight, K., Kauter, G., & McCorkell, B., (2012). Yield, development, and quality response of dual-toxin Bt cotton to Helicoverpa spp. infestations in Australia. Entomologia Experimentalis et Applicata, 145(1), 72–81. doi:10.1111/j.1570-7458.2012.01313.x
37. Luttrell, R. G., Teague, T. G., & Brewer, M. J., (2015). Cotton insect pest management. Cotton, 57, 509–546. doi:10.2134/agronmonogr57.2014.0072
38. Menozzi, P., Shi, M. A., Lougarre, A., Tang, Z. H., & Fournier, D., (2004). Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations. BMC Evolutionary Biology, 4, 4. doi:10.1186/1471-2148-4-4
39. Messaoudi, A., Belguith, H., & Ben Hamida, J., (2013). Homology modeling and virtual screening approaches to identify potent inhibitors of VEB-1 β-lactamase. Theoretical Biology & Medical Modelling, 10, 22. doi:10.1186/1742-4682-10-22
40. Naranjo, S. E., (2011). Impacts of Bt transgenic cotton on integrated pest management. Journal of Agricultural and Food Chemistry, 59(11), 5842–5851. doi:10.1021/jf102939c
41. Nauen, R., (2007). Insecticide resistance in disease vectors of public health importance. Pest Management Science, 63(7), 628–633. doi:10.1002/ps.1406
42. Neal, J. J., & Wu, W., (1994). Inhibition of insect cytochromes P450 by furanocoumarins. Pesticide Biochemistry and Physiology, 50(1), 43–50.
43. Onstad, D. W., (2014). Insect resistance management : Biology, economics, and prediction. (D. W., Onstad, Ed.) (2nd ed.). Boston, MA: Academic Press.
44. Roush, R., & Tabashnik, B., (1991). Pesticide Resistance in Arthropods. Boston, MA: Springer, US.
45. Ryckaert, J. P., Ciccotti, G., & Berendsen, H. J. C., (1977). Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341. doi:10.1016/0021-9991(77)90098-5
46. Sakthivel, S., & Habeeb, S. K. M., (2018). Combined pharmacophore, virtual screening and molecular dynamics studies to identify Bruton’s Tyrosine Kinase inhibitors. Journal of Biomolecular Structure and Dynamics, 0(ja), 1–56. doi:10.1080/07391102.2017.1415821
47. Schneeberger, K., Malde, K., Coward, E., & Jonassen, I., (2005). Masking repeats while clustering ESTs. Nucleic Acids Research, 33(7), 2176–2180. doi:10.1093/nar/gki511
48. Schüttelkopf, A. W., & van Aalten, D. M. F., (2004). PRODRG: A tool for high-throughput crystallography of protein–ligand complexes. Acta Crystallographica Section D: Biological Crystallography, 60(8), 1355–1363. doi:10.1107/S0907444904011679
49. Schwede, T., Kopp, J., Guex, N., & Peitsch, M. C., (2003). SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Research, 31(13), 3381–3385. doi:10.1093/nar/gkg520
50. Settle, W., Soumare, M., Sarr, M., Garba, M. H., & Poisot, A.-S., (2014). Reducing pesticide risks to farming communities: Cotton farmer field schools in Mali. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 369, 20120277. doi:10.1098/rstb.2012.0277
51. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S., (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729. doi:10.1093/molbev/mst197
52. Tian, J.-C., Yao, J., Long, L.-P., Romeis, J., & Shelton, A. M., (2015). Bt crops benefit natural enemies to control non-target pests. Scientific Reports, 5, e111629. doi:10.1038/srep16636
53. Tice, C. M., (2001). Selecting the right compounds for screening: Does Lipinski's Rule of 5 for pharmaceuticals apply to agrochemicals? Pest Management Science, 57(1), 3–16. doi:10.1002/1526-4998(200101)57:1<3::AID-PS269>3.0.CO;2-6
54. Tou, W. I., Chang, S., Lee, C., & Chen, C. Y., (2013). Drug design for neuropathic pain regulation from traditional Chinese medicine. Scientific Reports, 3, 2204. doi:10.1038/srep00844
55. Trapero, C., Wilson, I. W., Stiller, W. N., & Wilson, L. J., (2016). Enhancing integrated pest management in GM cotton systems using host plant resistance. Frontiers in Plant Science, 7, 500. doi:10.3389/fpls.2016.00500
56. Verma, P., Maurya, P., Tiwari, M., & Tiwari, V., (2017, December). In-silico interaction studies suggest RND efflux pump mediates polymyxin resistance in Acinetobacter baumannii. Journal of Biomolecular Structure and Dynamics, 1102,1–18. doi:10.1080/07391102.2017.1418680
57. Vontas, J. G., Hejazi, M. J., Hawkes, N. J., Cosmidis, N., Loukas, M., Janes, R. W., & Hemingway, J., (2003). Resistance-associated point mutations of organophosphate insensitive acetylcholinesterase, in the olive fruit fly Bactrocera oleae. Insect Molecular Biology, 11(4), 329–336. doi:10.1046/j.1365-2583.2002.00343.x
58. Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K., & Eppenberger, H. M., (1992). Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: The “phosphocreatine circuit” for cellular energy homeostasis. The Biochemical Journal, 21–40.10.1042/bj2810021
59. Wang, H. R., Zhu, W. J., & Wang, X. Y., (2011). Mechanism of inhibition of arginine kinase by flavonoids consistent with thermodynamics of docking simulation. International Journal of Biological Macromolecules, 49(5), 985–991. doi:10.1016/j.ijbiomac.2011.08.017
60. Wang, Z., Zhao, Z., Abou-Zaid, M. M., Arnason, J. T., Liu, R., Walshe-Roussel, B., … Scott, I. M., (2014). Inhibition of insect glutathione S-transferase (GST) by Conifer Extracts. Archives of Insect Biochemistry and Physiology, 87(4), 234–249. doi:10.1002/arch.21192
61. Whitehouse, M. E. A., Wilson, L. J., & Fitt, G. P., (2005). A comparison of arthropod communities in transgenic Bt and conventional cotton in Australia. Environmental Entomology, 34(5), 1224–1241.10.1093/ee/34.5.1224
62. Wilson, L., Downes, S., Khan, M., Whitehouse, M., Baker, G., Grundy, P., & Maas, S., (2013). IPM in the transgenic era: A review of the challenges from emerging pests in Australian cotton systems. Crop and Pasture Science, 64(8), 737–749. doi:10.1071/CP13070
63. Wu, X. Q., Zhu, W. J., Lü, Z. R., Xia, Y., Yang, J. M., Zou, F., & Wang, X. Y., (2009). The effect of rutin on arginine kinase: Inhibition kinetics and thermodynamics merging with docking simulation. International Journal of Biological Macromolecules, 44(2), 149–155. doi:10.1016/j.ijbiomac.2008.11.007
64. Yellapu, N. K., Gopal, J., Kasinathan, G., & Purushothaman, J., (2017). Molecular modelling studies of kdr mutations in voltage gated sodium channel revealed significant conformational variations contributing to insecticide resistance. Journal of Biomolecular Structure and Dynamics, 1–12, doi:10.1080/07391102.2017.1341338
65. Zhao, Y., Yang, G., Wang-Pruski, G., & You, M., (2008). Phyllotreta striolata (coleoptera: Chrysomelidae): Arginine kinase cloning and rnai-based pest control. European Journal of Entomology, 105(5), 815–822.10.14411/eje.2008.108